Human Movement Science 30 (2011) 648–657

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Human Movement Science

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Anticipatory and compensatory postural adjustments insitting in children with cerebral palsy

Aline Bigongiari a, Flávia de Andrade e Souza a, Patrícia Martins Franciulli a,Semaan El Razi Neto a, Rubens Correa Araujo a, Luis Mochizuki b,⇑a Laboratory of Biomechanics, University São Judas Tadeu, Brazilb Escola de Artes, Ciências, e Humanidades, Universidade de Sao Paulo, Avenida Arlindo Bétio, 1000 São Paulo, SP 03828 000, Brazil

a r t i c l e i n f o

Article history:Available online 31 March 2011

PsycINFO classification:25203297

Keywords:Anticipatory postural adjustmentCerebral palsyPostural control

0167-9457/$ - see front matter � 2011 Elsevier B.Vdoi:10.1016/j.humov.2010.11.006

⇑ Corresponding author.E-mail address: alinebigongiari@usp.br (L. Moch

a b s t r a c t

The aim of this study was to examine postural control in childrenwith cerebral palsy performing a bilateral shoulder flexion to graspa ball from a sitting posture. The participants were 12 typicallydeveloping children (control) without cerebral palsy and 12 childrenwith cerebral palsy (CP). We analyzed the effect of ball mass (1 kgand 0.18 kg), postural adjustment (anticipatory, APA, and compen-satory, CPA), and groups (control and CP) on the electrical activityof shoulder and trunk muscles with surface electromyography(EMG). Greater mean iEMG was seen in CPA, with heavy ball, andfor posterior trunk muscles (p < .05). The children with CP presentedthe highest EMG and level of co-activation (p < .05). Linear regres-sion indicated a positive relationship between EMG and aging forthe control group, whereas that relationship was negative for partic-ipants with CP. We suggest that the main postural control strategy inchildren is based on corrections after the beginning of the move-ment. The linear relationship between EMG and aging suggests thatpostural control development is affected by central nervous diseasewhich may lead to an increase in muscle co-activation.

� 2011 Elsevier B.V. All rights reserved.

1. Introduction

Adequate postural control is necessary for an appropriate voluntary movement performance (Liao,Yang, Hsu, Chan, & Wei, 2003; Rose et al., 2002; Woollacott et al., 1998). Lobo and Galloway (2008)

. All rights reserved.

izuki).

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showed that infants with postural experience likely had improved head and trunk strength and con-trol for visual exploration and reaching, had more appropriate muscle responses to maintain balance,and had increased perceptual-motor experiences in a variety of positions. Therefore, these authorsconsidered factors both internal (age and development) and external (environment) to the infants.However, different problems affect movement performance, such as motor disorders (Levin, Cirstea,Archambault, Son, & Roby-Brami, 2002; Mewasinh et al., 2002) or neuromuscular injuries (Roseet al., 2002; Woollacott; 2002).

Cerebral palsy (CP) is a non-progressive motor disorder caused by development damage or animmature brain which leads to impaired postural control (Gianni, 2005; Rose et al., 2002). Severalneural factors constrain balance control in children with CP: spasticity, hyperactive stretch reflexes,and problems with muscle coordination including poorly organized postural responses and increasedmuscle coactivation at individual joints (Woollacott et al., 1998). Dynamic balance control includesproactive or anticipatory postural adjustments (APA), and reactive or compensatory postural adjust-ments (CPA) to enhance balance (Aruin, 2003; Massion, 1998). By APA we mean movements that re-duce the effects of a perturbation to posture caused by voluntary control. On the other hand, CPA arereactive responses to postural perturbations. Since CP children may have significant balance problems,an evaluation of both APA and CPA seems warranted.

Several changes occur in the postural control of children with CP. During reaching, children with CPshow direction-specific postural adjustments (Hadders-Algra, van der Fits, Stremmelaar, & Touwen,1999; van der Heide et al., 2004) and during standing they show abnormalities in muscle timingand increased levels of coactivation (Brogren, Hadders-Algra, & Forssberg, 1996; Woollacott et al.,1998). Postural control develops differently in children with and without CP. While standing balanceusually improves with age in typically developing children, it does not improve with age in childrenwith CP (Rose et al., 2002; Shumway-Cook, Hutchinson, Kartin, Price, & Woollacott, 2003). The APAduring reaching in sitting posture in typically developing children is consistently present from15 months of age onwards (van der Fits, Otten, Klip, van Eykern, & Hadders-Algra, 1999). However,in children with CP, the APA during reaching while sitting is variable in its development (Roseet al., 2002; Woollacott et al., 1998). Both children (without and with CP) show a large variation inthe neck and trunk muscles activation latencies (van der Heide et al., 2004). Children with moderateand serious outcomes due to CP show visible deficits in postural control. Their motor and functionalcapacities need to be improved for the maintenance of standing and sitting position through the headand trunk stabilization and alignment (Liao, Yang, Hsu, Chan, & Wei, 2003).

The variety of results across different experiments and the lack of postural studies in sitting posi-tion take us to this question: how do central motor disorders affect the postural adjustments? In orderto answer this question, the main purpose of this study was to investigate the postural adjustments inchildren with CP performing shoulder flexion to grasp a ball. We compared the postural adjustmentsacross different groups and task conditions to test if the importance of anticipatory and compensatoryadjustments performed by children with and without CP to postural control are different. We hypoth-esized that there would be a difference in the anticipatory and compensatory postural adjustmentsbetween the children with CP and typically developing children. The children with CP have less antic-ipatory and greater compensatory adjustments.

2. Methods

2.1. Participants

The participants in this study were 12 typically developing children (4 boys and 8 girls) and 12spastic diplegic children (6 boys and 6 girls). Their main characteristics are presented in Table 1.The typically developing children were recruited from physiotherapy undergraduate students’ rela-tives who were without any physical or neurological problems and they served as control group.The spastic diplegic children served as the experimental group (CP). The children with CP were re-cruited from the physiotherapy service of the University. All parents gave informed consent accordingto the procedures approved by the Office for Regulatory Compliance of the Institution.

Table 1The description of the main characteristics of the participants (GMFCS scale, sex, age, weight and height), divided into controlgroup (children without CP) and children with CP.

Participants Sex Group GMFCS Age (year) Weight (kg) Height (m)

1 Girl CP III 7 20.4 1.112 Boy CP I 8 21.5 1.193 Boy CP II 8 22.0 1.194 Boy CP III 8 25.2 1.205 Girl CP II 8 22.8 1.226 Boy CP III 9 28.4 1.297 Girl CP III 9 28.5 1.268 Girl CP I 9 30.7 1.429 Boy CP I 9 27.6 1.30

10 Girl CP I 10 29.9 1.3311 Boy CP III 11 28.8 1.2612 Girl CP III 11 41.0 1.4013 Boy Control – 7 24.0 1.2314 Girl Control – 8 25.2 1.2515 Girl Control – 8 25.9 1.2516 Girl Control – 9 28.2 1.2917 Boy Control – 9 29.0 1.3318 Girl Control – 9 30.1 1.3619 Girl Control – 10 31.6 1.3820 Boy Control – 10 34.5 1.3921 Boy Control – 10 36.2 1.4222 Girl Control – 11 37.3 1.4523 Girl Control – 11 38.3 1.4424 Girl Control – 11 40.5 1.46

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The inclusion criteria for the control group were: (1) to be between 7 and 11 years old and (2) topresent typical physical and motor developing condition. The exclusion criteria for the control groupwere: (1) to have any physical, motor and cognitive impairment and (2) to be unable to understandthe instructions to perform the motor task. On the other hand, to be included in the experimentalgroup, children with CP had to be able to stand in the sitting position by itself and to grasp a throwingball with their both hands and to be between 7 and 11 years old. The exclusion criteria for the exper-imental group were: to be unable to understand the instructions to perform the motor task; be receiv-ing Botox treatments up to six months ago, and to be unable to sit and stand quiet without anyexternal assistance.

2.2. Procedure

One senior physiotherapist performed the GMFCS test at the CP children group. When she per-formed the tests she was not aware of the hypothesis of this study.

For the experimental trials, the participants sat on a stable bed without back or foot support. Theywere instructed to grasp a thrown ball with both hands. The participants were instructed to hold theirarms at their sides. After a warning signal, they were told to raise their arms and grasp the ball withtheir arms parallel to the floor. After the children had grasped the ball, the raw signal was observedand only the signal, that demonstrated APA, was recorded. Two criteria were important: 1 – to graspa thrown ball and 2 – to show APA. The order of the ball conditions was randomized across partici-pants. In each ball condition, 10 practice trials were given to familiarize the children with the task.The 10 practice trials were enough for all participants. Some children had learned before to complete10 trials, but additional trials were not necessary for any of the participants. For each ball (light andheavy), 10 successful measurement trials were performed (van der Heide, Otten, van Eykern, &Hadders-Algra, 2003; Morris & Allison, 2006; Yiou, Schneider, & Roussel, 2007) and recorded. In bothball conditions, the children were aware of the mass of the ball.

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2.3. Data processing and statistical analysis

The electromyographic signals (EMG) were recorded with bipolar surface electrodes (Myosystem1400, Noraxon Inc., Scottsdale, Arizona, USA) on the following muscles: anterior deltoid (DE), bicepsbrachii (BB), sternocleidomastoid (SC), neck extensor (NE – level C7), thoracic extensor (TE – levelT10), lumbar extensor (LE – level L3), and rectus abdominis (RA). The beginning of movement was de-tected with a bi-dimensional flexible electrogoniometer (Noraxon Inc., Scottsdale, Arizona, USA). Theaxes of the electrogoniometer were aligned to the center of shoulder rotation. Two balls of the samesize were thrown to the children (light: 0.180 kg and heavy: 1 kg). All data were collected on a micro-computer via an A/D converter. Data sampling was accomplished at 1000 Hz.

The EMG data were amplified 1000 times and band-pass filtered (10–200 Hz) using a 4th orderButterworth filter. The angular position data were low-pass filtered (20 Hz) using a 4th order Butter-worth filter. The filtered EMG was then full-wave rectified. The integrated signals (iEMG) were calcu-lated for each task and muscle at two time windows. For APA, the window began 200 ms before theinitiation of movement to 50 ms after the initiation of movement (see Fig. 1). For CPA, the integrationwindow ranged from 50 ms after movement initiation to 300 ms after movement initiation. iEMGranging from 400 ms before movement initiation to 300 ms before movement initiation was referredto as pre-APA. The times defining both APA and CPA were derived from previous literature (Shiratori &Latash, 2000).

The iEMG during the pre-APA period was subtracted from the APA period to remove the baselineiEMG activity. We normalized iEMG of each muscle by its maximum value and classified it into threeEMG levels of activity: mild, from 0% to 30%; moderate, from 30% to 70%; and strong, from 70 to 100%.

2.4. Variables

For the description and analysis of postural control of the control and experimental groups, weused the following variables:

(a) The intensity of muscular activation: the iEMG was calculated during the APA and the CPA forthe selected muscles.

(b) The degree of reciprocal inhibition: the iEMG activity of the dorsal muscles (LE, NE) was sub-tracted from the ventral muscles (RA, SC) to determine the degree of reciprocal inhibition (R).

Fig. 1. Schematic indicating the definitions for anticipatory (APA) and compensatory (CPA) postural adjustments. The top graphindicates the angular position of the shoulder while the bottom graph illustrates a typical EMG time pattern. The dot lines showthe time limits of APA, CPA and pre-APA.

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(c) The amount of co-contraction: the iEMG activity of the muscle pairs RA-LE and SE-NE wereadded to represent the amount of co-contraction (C).

The children with CP were classified within Gross Motor Function Classification System for CerebralPalsy (GMFCS) (Palisano et al., 1997). Each individual result is presented in Table 1. This scale is ap-plied to classify the participants’ functional abilities (level I: participant walks without restrictionsand has restriction to perform more advanced gross motor skills; level II: participant walks withoutassistive devices and has limitation to walk outside; and level III: participant needs assistive mobilitydevices to walk and has constraints to walk outside).

Multiple Analysis of Variance (MANOVA) was applied to verify the effect of postural adjustment(APA and CPA), group (control and CP), ball (light and heavy) and muscle (DE, SC, NE, TE, LE, BB,and RA). Tukey’s HSD was applied for post-hoc comparisons where appropriate. Multiple linear regres-sion analysis was applied to test the relationship between the iEMG of the trunk muscles and aging.Lastly, multiple linear regression analysis was performed between GMFCS scale and postural adjust-ment (APA and CPA).

3. Results

iEMG amplitude during APA increased compared to the resting level in four muscles (DE, SC, TE,and LE) during both the light and heavy ball conditions in both the control and CP groups (Table 2).The rectus abdominus (RA) decreased compared to the resting level in the light ball condition ofthe control group and in both ball conditions of the CP group. Both the BB and the NE muscles de-creased in the light ball condition of the control group and heavy ball condition of the CP grouprespectively.

The magnitudes of the iEMG for postural adjustment, group, ball and muscles are presented inFig. 2. The MANOVA on these effects indicated that there were no significant interactions in this anal-ysis. We found that all factors affected iEMG (p < .001). That is, the iEMG magnitude was greater forthe CPA than the APA, the CP group than the control and the heavy ball than the light ball. Thepost-hoc analysis revealed the highest iEMG for SC, TE, and LE muscles (p < .001).

The mean values of both the co-contraction (C) and reciprocal inhibition (R) indices are presentedin Table 3. For both indices, there were no significant interactions between postural adjustment, groupand ball. However, there was a significant difference between the main effects of postural adjustment(APA versus CPA), group (control versus CP), and ball (light versus heavy) (p < .0001) for both the neckand trunk muscles. The R index was significantly different between groups (control and CP) (p < .001)for both the trunk and the neck. The highest R index was found for the trunk muscles and for thecontrol group versus the CP group.

MANOVA was used to verify the effect of postural adjustment (APA and CPA), ball (light and heavy),group (control and CP), and EMG activity level (mild, moderate, and strong) on frequency distribution

Table 2Anticipatory postural adjustment (APA) across muscles (deltoid, sternocleidomastoid, neck extensor, thoracal extensor, lumbarextensor, biceps brachii and rectus abdominis) for the control and cerebral palsy groups during catching a light or heavy ball. Cross(+) means that activity during APA is higher than pre-APA, while trace (�) means that activity during APA is smaller than pre-APA.

Type of anticipatory postural adjustment

Group Control group Cerebral palsy group

Ball mass Light Heavy Light Heavy

Muscle Deltoid + + + +Sternocleidomastoid + + + +Neck extensor + + + �Thoracal extensor + + + +Lumbar extensor + + + +Biceps brachii � + + +Rectus abdominis � + � �

Fig. 2. Average iEMG (SD) during anticipatory (APA) and compensatory (CPA) postural adjustments for the muscles of the (a)control and (b) cerebral palsy groups when catching a light or heavy ball. The muscles were anterior deltoid (DE), biceps brachii(BB), sternocleidomastoid (SC), neck extensor (NE), thoracic extensor (TE), lumbar extensor (LE), and rectus abdominis (RA).

Table 3Neck and trunk co-contraction (C) and reciprocal inhabitation (R) indexes during anticipatory (APA) and compensatory (CPA)postural adjustments for the control and cerebral palsy groups when catching a light or heavy ball.

iEMG (% mean)

Cerebral palsy Control

APA CPA APA CPA

Light Heavy Light Heavy Light Heavy Light Heavy

Neck C-index 38.0 ± 11 42.8 ± 10 51.9 ± 12 54.0 ± 10 41.0 ± 12 40.1 ± 12 53.4 ± 10 51.5 ± 10R-index 5.3 ± 4.2 5.8 ± 4.9 9.3 ± 8.9 8.0 ± 6.6 6.6 ± 4.4 7.3 ± 6.2 6.7 ± 5.4 7.7 ± 7.1

Trunk C-index 19.0 ± 9.6 44.9 ± 20 58.2 ± 18 56.9 ± 17 47.0 ± 23 44.8 ± 21 52.5 ± 17 56.2 ± 18R-index 18.3 ± 9.1 10.6 ± 10 13.7 ± 10 12.2 ± 10 10.6 ± 11 11.5 ± 9.3 10.1 ± 10 12.6 ± 9.1

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of postural responses. This analysis was based on data presented in Fig. 3. There were significant inter-actions between muscle activity level and the effects of postural adjustment, ball and group(p < .0001). For mild activity, responses were more frequently with heavy ball, and for control group.For moderate activity, responses were more frequent during CPA and with light ball. For strong activ-ity, responses were more frequent during CPA with light ball and for the CP group. The post hoc anal-ysis indicated that mild activity was the most frequent response while the least frequent response wasat the strong level (p < .0001).

A multiple linear regression analysis was used to verify the relationship between muscular activityand aging (Fig. 4). For the control group, a positive linear relationship between iEMG and aging duringAPA was found (R2 = .28, p = .001) and a negative relationship during CPA (R2 = .14, p = .02). For the CPgroup, a negative relationship between iEMG and aging during APA and CPA (R2 = .39, p = .0001).

Fig. 3. The muscle activity level during postural adjustments and groups. The muscle activity is presented according to itsfrequency distribution of iEMG divided into three levels (0–30%, 30–70%, and 70–100%) during (a) compensatory (CPA) and (b)anticipatory (APA) postural adjustments for the control and cerebral palsy groups during catching a light or heavy ball.

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The GMFCS test resulted in four children (33.3%) classified at level I, two children (16.6%) at level II,and six children (50%) were classified at level III. A regression analysis indicated no relationship be-tween functional ability and APA (R = �.04, p = .87) or APC (R = �.21, p = .46).

4. Discussion

The purpose of this study was to compare anticipatory and compensatory postural adjustments inindividuals with CP and typically developing children. We hypothesized that children with CP wouldhave less anticipatory and greater compensatory adjustments than healthy children. In general, wefound differences in muscle activity to support our hypothesis.

Typically developing children and children with CP raised their arms to catch a ball using differentmuscular patterns of muscle activation. Mostly, muscle activity increased before this movement fortypically developing children (i.e., APA); however, some muscles were tuned differently across groupand task conditions. Typically developing children, as well as young adults, show changes in posturaladjustments with additional load (Hadders-Algra et al., 1999; Witherington et al., 2002), leading to anincreased APA intensity (Bouisset, Richardson, & Zattara, 2000; Vernazza-Martin, Martin, Cincera, &Pedotti, 1999). To catch a more massive ball, our typically developing children increased the activityof all muscles while children with CP tuned some muscles (DE, SC, TE, LE, and BB) and relaxed others(NE and RA).

To achieve the postural goal (control of balance) during a motor task, different strategies are ap-plied prior to and/or after the initiation of the movement. The muscle activities are constrained bysynergies that help to increase or decrease the task success; therefore, we can identify good or badsynergies. How muscles are switched on or off to accomplish the task can help us to reveal the

Fig. 4. The main results of multiple linear regression analysis of iEMG of all muscles (deltoid, biceps brachii, sternocleido-mastoid, neck extensor, thoracal extensor, lumbar extensor, and rectus abdominis), during anticipatory (APA) andcompensatory (CPA) postural adjustments for the control and cerebral palsy groups during catching a ball.

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postural synergy organization. Considering all task repetitions, the children with CP and typicallydeveloping children activated their muscles during APA. The stronger activations were often observedafter the initiation of movement when the mass ball was heavy for the children with CP while typicallydeveloping children activated their muscles at mild level. Thus, there were different uses of synergiesleading to different patterns of activation between groups.

We found that children with CP presented stronger single and agonist/antagonist muscle activa-tions than typically developing children. The lack of supraspinal modulation on tonic stretch reflexthresholds at segmental levels, spasticity, or central nervous system (CNS) immaturity (Brogrenet al., 1996; van der Fits and Hadders-Algra; 1998) are common in children with CP and contributeto strong single muscle responses. As a consequence, those neural problems lead to poorly organizedpostural responses, including increased muscle coactivation at individual joints and movementrestrictions (Aruin & Almeida, 1997; Brogren et al., 1996; Dan et al., 2000, Hadders-Algra et al.,1999; Levin et al., 2002; Woollacott, 2002; Woollacott et al., 1998). Delays in the development of spe-cific neural or musculoskeletal subsystem and sensorial deficits contribute to balance difficulties(Hadders-Algra et al., 1999; van der Heide et al., 2004; Woollacott, 2002).

Our results did not show a linear relationship between GMFCS scale and postural adjustmentacross participants. The lack of a relationship between functional levels and postural control suggeststhat more specific scales to describe balance and upper limb movements are necessary. After all, qual-itative analyses of standing and gait cannot account for other motor abilities.

Maturity and motor experiences improve motor development (Hadders-Algra et al., 1999) and bothprocesses are improved by aging. In fact, postural adjustments change as people get older (Grasso,Assaiante, Prévost, & Berthoz, 1998; Hay & Redon, 1999; Mercer & Sahrmann, 1997; van der Fits &Hadders-Algra, 1998; Woollacott et al., 1998; Witherington et al., 2002). This occurs because partici-pants learn how to use postural adjustments to better achieve the task goals or to avoid postural risksassociated with movement perturbation. In this sense, infants develop APA while they learn to get up,stand up, and walk (van der Fits et al., 1999; Witherington et al., 2002). In our results, for typically

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developing children, regression analysis, although producing weak correlations, seemed to indicatetwo postural processes with aging: APA increases, while CPA decreases.

For children with CP, aging affects postural processes in a different fashion. Although children withCP had more difficulty in grasping the thrown ball, they also caught it. Contrary to typically developingchildren, the children with CP decreased both APA and CPA with aging. Facing the task, both feedfor-ward and feedback control may be weakened due to aging and the progression of the disease.Although no specific-direction muscle activation has been observed in children with CP, probably be-cause only severe children with CP show changes in the specific-direction postural responses (Brogrenet al., 1996; van der Fits & Hadders-Algra, 1998; van der Heide et al., 2003). In addition, the main prob-lem in a CNS lesion is the fine modulation (temporal and tonic patterns) of postural responses (van derHeide et al., 2004) which may have contributed to the decline in both APA and CPA activities acrossages in this study.

In conclusion, typically developing children and children with CP showed different patterns of pos-tural activity across load perturbation. As children with CP performed the task with lower muscleactivity, efforts should be made to guarantee that such condition does not lead to the increase of pos-tural instability and unbalance situations in daily life activities. We believe the relationship betweenpostural control and development in children with cerebral palsy shows us that on-going functionalactivity training and neuromuscular rehabilitation are necessary to deal with cerebral palsy impair-ment. However, to improve postural and motor control, multisensory stimulation tasks should beencouraged during rehabilitation programs.

We only showed how the intensity of muscle changes across the experimental conditions. Furtheranalysis is necessary to verify whether muscular latency is different between children with and with-out CP. This information may be interesting in view of the discussion about how those children coor-dinates several muscles to perform a postural and movement task.

Acknowledgments

The authors gracefully acknowledge Joseph Hamill for his invaluable suggestions and discussionsand the anonymous reviewers for their helpful comments.

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